Trade-offs among immune mechanisms: bacterial-challenged Spodoptera frugiperda larvae reduce nodulation reactions during behavioral fever

Authors: ZHANG, LEI - Chinese Academy Of Agricultural Sciences; Goodman, Cynthia; Ringbauer, Joseph - Joe; JIANG, XING-FU - Chinese Academy Of Agricultural Sciences; LV, WEIXIANG - China West Normal University; XIE, DIANJIE - Chinese Academy Of Agricultural Sciences; REALL, TAMRA - University Of Missouri; Stanley, David

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2023
Publication Date: 11/9/2023
Citation: Zhang, L., Goodman, C.L., Ringbauer Jr, J.A., Jiang, X., Lv, W., Xie, D., Reall, T., Stanley, D.W. 2023. Trade-offs among immune mechanisms: bacterial-challenged Spodoptera frugiperda larvae reduce nodulation reactions during behavioral fever. Insects. 14(11):864. https://doi.org/10.3390/insects14110864.
DOI: https://doi.org/10.3390/insects14110864

Interpretive Summary: Insect immunity is a system that effectively protects insects from fungal, viral, bacterial and parasitic infections. A problem is that deployment of individual immune actions within the overall system and the signaling mechanisms that mediate the deployments are not well understood. One specific immune action is to deploy insect blood cells to directly aggregate and kill invaders. This is a costly defense reaction because many blood cells are lost in the process and must be replaced. Another immune action is to generate a behavioral fever by adopting postures that maximize exposure to the sun. In this paper we report on our discovery that under appropriate settings, caterpillars of a pest moth that are given an opportunity to generate behavioral fevers will reduce their deployment of blood cells to directly aggregate and kill invaders. That is, the caterpillars trade deploying blood cells for fevers is the specific situation is consistent with behavioral fever. We also identified a specific chemical that mediates the behavioral fevers. After we blocked the chemical and gave the caterpillars a standard infection, we found the caterpillars did not generate fevers. This new information will help scientists working around the globe improve agricultural productivity by enhancing our understanding of insect immunity and improving use of biological control programs to produce attractive and healthy goods for a growing human population.

Technical Abstract: Insect innate immunity is composed of cellular and humoral immunity, the former acting via circulating hemocytes and the latter via production of antimicrobial proteins and phenol oxidase-driven melanization. Cellular immunity is the first response, responsible for clearing most infections from hemolymph during the first two h post infection. Beyond these, some insects reduce pathogen loads by behavioral fever. The effective aspects of fever tend to obscure some of its subtle features. In some species, fever itself can be detrimental. Lethal temperatures of some invaders can be higher than their hosts and fever would not be adaptive. Some species exhibit pathogen specificity in fever reactions. Most insect species exhibit behavioral fever by moving to warmer sites within their habitats or assuming postures that increase exposure to heat sources. We reasoned that behavioral fevers are based on posturing and they would be a relatively low-cost immune function compared to hemocyte-driven nodule formation, which involves loss and replacement of many hemocytes. On this reasoning, we posed the hypothesis that expensive hemocyte-based immunity is traded off for behavioral fevers in infected larvae of the fall army worm, Spodoptera frugiperda. Here, we report that febrile larvae produced far fewer nodules compared to controls.